Estimating neural activity from visual areas using functionally defined EEG templates.

Electroencephalography (EEG) is a common and inexpensive method to record neural activity in humans. However, it lacks spatial resolution making it difficult to determine which areas of the brain are responsible for the observed EEG response. Here we present a new easy-to-use method that relies on EEG topographical templates. Using MRI and fMRI scans of 50 participants, we simulated how the activity in each visual area appears on the scalp and averaged this signal to produce functionally defined EEG templates. Once created, these templates can be used to estimate how much each visual area contributes to the observed EEG activity. We tested this method on extensive simulations and on real data. The proposed procedure is as good as bespoke individual source localization methods, robust to a wide range of factors, and has several strengths. First, because it does not rely on individual brain scans, it is inexpensive and can be used on any EEG data set, past or present. Second, the results are readily interpretable in terms of functional brain regions and can be compared across neuroimaging techniques. Finally, this method is easy to understand, simple to use and expandable to other brain sources.

Three-Dimensional Motion Perception: Comparing Speed and Speed Change Discrimination for Looming Stimuli.

Judging the speed of objects moving in three dimensions is important in our everyday lives because we interact with objects in a three-dimensional world. However, speed perception has been seldom studied for motion in depth, particularly when using monocular cues such as looming. Here, we compared speed discrimination, and speed change discrimination, for looming stimuli, in order to better understand what visual information is used for these tasks. For the speed discrimination task, we manipulated the distance and duration information available, in order to investigate if participants were specifically using speed information. For speed change discrimination, total distance and duration were held constant; hence, they could not be used to successfully perform that task. For the speed change discrimination task, our data were consistent with observers not responding specifically to speed changes within an interval. Instead, they may have used alternative, arguably less optimal, strategies to complete the task. Evidence suggested that participants used a variety of cues to complete the speed discrimination task, not always solely relying on speed. Further, our data suggested that participants may have switched between cues on a trial to trial basis. We conclude that speed changes in looming stimuli were not used in a speed change discrimination task, and that naïve participants may not always exclusively use speed for speed discrimination.

Neural responses to apparent motion can be predicted by responses to non-moving stimuli.

When two objects are presented in alternation at two locations, they are seen as a single object moving from one location to the other. This apparent motion (AM) percept is experienced for objects located at short and also at long distances. However, current models cannot explain how the brain integrates information over large distances to create such long-range AM. This study investigates the neural markers of AM by parcelling out the contribution of spatial and temporal interactions not specific to motion. In two experiments, participants' EEG was recorded while they viewed two stimuli inducing AM. Different combinations of these stimuli were also shown in a static context to predict an AM neural response where no motion is perceived. We compared the goodness of fit between these different predictions and found consistent results in both experiments. At short-range, the addition of the inhibitory spatial and temporal interactions not specific to motion improved the AM prediction. However, there was no indication that spatial or temporal non-linear interactions were present at long-range. This suggests that short- and long-range AM rely on different neural mechanisms. Importantly, our results also show that at both short- and long-range, responses generated by a moving stimulus could be well predicted from conditions in which no motion is perceived. That is, the EEG response to a moving stimulus is simply a combination of individual responses to non-moving stimuli. This demonstrates a dissociation between the brain response and the subjective percept of motion.

Speed change discrimination for motion in depth using constant world and retinal speeds.

Motion at constant speed in the world maps into retinal motion very differently for lateral motion and motion in depth. The former is close to linear, for the latter, constant speed objects accelerate on the retina as they approach. Motion in depth is frequently studied using speeds that are constant on the retina, and are thus not consistent with real-world constant motion. Our aim here was to test whether this matters: are we more sensitive to real-world motion? We measured speed change discrimination for objects undergoing accelerating retinal motion in depth (consistent with constant real-world speed), and constant retinal motion in depth (consistent with real-world deceleration). Our stimuli contained both looming and binocular disparity cues to motion in depth. We used a speed change discrimination task to obtain thresholds for conditions with and without binocular and looming motion in depth cues. We found that speed change discrimination thresholds were similar for accelerating retinal speed and constant retinal speed and were notably poor compared to classic speed discrimination thresholds. We conclude that the ecologically valid retinal acceleration in our stimuli neither helps, nor hinders, our ability to make judgements in a speed change discrimination task.

Sparse EEG/MEG source estimation via a group lasso.

Non-invasive recordings of human brain activity through electroencephalography (EEG) or magnetoencelphalography (MEG) are of value for both basic science and clinical applications in sensory, cognitive, and affective neuroscience. Here we introduce a new approach to estimating the intra-cranial sources of EEG/MEG activity measured from extra-cranial sensors. The approach is based on the group lasso, a sparse-prior inverse that has been adapted to take advantage of functionally-defined regions of interest for the definition of physiologically meaningful groups within a functionally-based common space. Detailed simulations using realistic source-geometries and data from a human Visual Evoked Potential experiment demonstrate that the group-lasso method has improved performance over traditional ℓ2 minimum-norm methods. In addition, we show that pooling source estimates across subjects over functionally defined regions of interest results in improvements in the accuracy of source estimates for both the group-lasso and minimum-norm approaches.

The steady-state visual evoked potential in vision research: A review.

Periodic visual stimulation and analysis of the resulting steady-state visual evoked potentials were first introduced over 80 years ago as a means to study visual sensation and perception. From the first single-channel recording of responses to modulated light to the present use of sophisticated digital displays composed of complex visual stimuli and high-density recording arrays, steady-state methods have been applied in a broad range of scientific and applied settings.The purpose of this article is to describe the fundamental stimulation paradigms for steady-state visual evoked potentials and to illustrate these principles through research findings across a range of applications in vision science.

The effect of contrast polarity reversal on face detection: evidence of perceptual asymmetry from sweep VEP.

Contrast polarity inversion (i.e., turning dark regions light and vice versa) impairs face perception. We investigated the perceptual asymmetry between positive and negative polarity faces (matched for overall luminance) using a sweep VEP approach in the context of face detection (Journal of Vision 12 (2012) 1-18). Phase-scrambled face stimuli alternated at a rate of 3 Hz (6 images/s). The phase coherence of every other stimulus was parametrically increased so that a face gradually emerged over a 20-s stimulation sequence, leading to a 3 Hz response reflecting face detection. Contrary to the 6 Hz response, reflecting low-level visual processing, this 3 Hz response was larger and emerged earlier over right occipito-temporal channels for positive than negative polarity faces. Moreover, the 3 Hz response emerged abruptly to positive polarity faces, whereas it increased linearly for negative polarity faces. In another condition, alternating between a positive and a negative polarity face also elicited a strong 3 Hz response, indicating an asymmetrical representation of positive and negative polarity faces even at supra-threshold levels (i.e., when both stimuli were perceived as faces). Overall, these findings demonstrate distinct perceptual representations of positive and negative polarity faces, independently of low-level cues, and suggest qualitatively different detection processes (template-based matching for positive polarity faces vs. linear accumulation of evidence for negative polarity faces).

How to use fMRI functional localizers to improve EEG/MEG source estimation.

EEG and MEG have excellent temporal resolution, but the estimation of the neural sources that generate the signals recorded by the sensors is a difficult, ill-posed problem. The high spatial resolution of functional MRI makes it an ideal tool to improve the localization of the EEG/MEG sources using data fusion. However, the combination of the two techniques remains challenging, as the neural generators of the EEG/MEG and BOLD signals might in some cases be very different. Here we describe a data fusion approach that was developed by our team over the last decade in which fMRI is used to provide source constraints that are based on functional areas defined individually for each subject. This mini-review describes the different steps that are necessary to perform source estimation using this approach. It also provides a list of pitfalls that should be avoided when doing fMRI-informed EEG/MEG source imaging. Finally, it describes the advantages of using a ROI-based approach for group-level analysis and for the study of sensory systems.

The evolution of a disparity decision in human visual cortex.

We used fMRI-informed EEG source-imaging in humans to characterize the dynamics of cortical responses during a disparity-discrimination task. After the onset of a disparity-defined target, decision-related activity was found within an extended cortical network that included several occipital regions of interest (ROIs): V4, V3A, hMT+ and the Lateral Occipital Complex (LOC). By using a response-locked analysis, we were able to determine the timing relationships in this network of ROIs relative to the subject's behavioral response. Choice-related activity appeared first in the V4 ROI almost 200 ms before the button press and then subsequently in the V3A ROI. Modeling of the responses in the V4 ROI suggests that this area provides an early contribution to disparity discrimination. Choice-related responses were also found after the button-press in ROIs V4, V3A, LOC and hMT+. Outside the visual cortex, choice-related activity was found in the frontal and temporal poles before the button-press. By combining the spatial resolution of fMRI-informed EEG source imaging with the ability to sort out neural activity occurring before, during and after the behavioral manifestation of the decision, our study is the first to assign distinct functional roles to the extra-striate ROIs involved in perceptual decisions based on disparity, the primary cue for depth.

Flies and humans share a motion estimation strategy that exploits natural scene statistics.

Sighted animals extract motion information from visual scenes by processing spatiotemporal patterns of light falling on the retina. The dominant models for motion estimation exploit intensity correlations only between pairs of points in space and time. Moving natural scenes, however, contain more complex correlations. We found that fly and human visual systems encode the combined direction and contrast polarity of moving edges using triple correlations that enhance motion estimation in natural environments. Both species extracted triple correlations with neural substrates tuned for light or dark edges, and sensitivity to specific triple correlations was retained even as light and dark edge motion signals were combined. Thus, both species separately process light and dark image contrasts to capture motion signatures that can improve estimation accuracy. This convergence argues that statistical structures in natural scenes have greatly affected visual processing, driving a common computational strategy over 500 million years of evolution.

On determining the intracranial sources of visual evoked potentials from scalp topography: a reply to Kelly et al. (this issue).

The cruciform model posits that if a Visual Evoked Potential component originates in cortical area V1, then stimuli placed in the upper versus lower visual field will generate responses with opposite polarity at the scalp. In our original paper (Ales et al., 2010b) we showed that the cruciform model provides an insufficient criterion for identifying V1 sources. This conclusion was reached on the basis of simulations that used realistic 3D models of early visual areas to simulate scalp topographies expected for stimuli of different sizes and shapes placed in different field locations. The simulations indicated that stimuli placed in the upper and lower visual field produce polarity inverting scalp topographies for activation of areas V2 and V3, but not for area V1. As a consequence of the non-uniqueness of the polarity inversion criterion, we suggested that past studies using the cruciform model had not adequately excluded contributions from sources outside V1. In their comment on our paper, Kelly et al. (this issue) raise several concerns with this suggestion. They claim that our initial results did not use the proper stimulus locations to constitute a valid test of the cruciform model. Kelly et al., also contend that the cortical source of the initial visually evoked component (C1) can be identified based on latency and polarity criteria derived from intracranial recordings in non-human primates. In our reply we show that simulations using the suggested critical stimulus locations are consistent with our original findings and thus do not change our conclusions regarding the use of the polarity inversion criterion. We further show that the anatomical assumptions underlying the putatively optimal locations are not consistent with available V1 anatomical data. We then address the non-human primate data, describing how differences in stimuli across studies and species confound an effective utilization of the non-human primate data for interpreting human evoked potential responses. We also show that, considered more broadly, the non-human primate literature shows that multiple visual areas onset simultaneously with V1. We suggest several directions for future research that will further clarify how to make the best use of scalp data for inferring cortical sources.

The time course of shape discrimination in the human brain.

The lateral occipital cortex (LOC) activates selectively to images of intact objects versus scrambled controls, is selective for the figure-ground relationship of a scene, and exhibits at least some degree of invariance for size and position. Because of these attributes, it is considered to be a crucial part of the object recognition pathway. Here we show that human LOC is critically involved in perceptual decisions about object shape. High-density EEG was recorded while subjects performed a threshold-level shape discrimination task on texture-defined figures segmented by either phase or orientation cues. The appearance or disappearance of a figure region from a uniform background generated robust visual evoked potentials throughout retinotopic cortex as determined by inverse modeling of the scalp voltage distribution. Contrasting responses from trials containing shape changes that were correctly detected (hits) with trials in which no change occurred (correct rejects) revealed stimulus-locked, target-selective activity in the occipital visual areas LOC and V4 preceding the subject's response. Activity that was locked to the subjects' reaction time was present in the LOC. Response-locked activity in the LOC was determined to be related to shape discrimination for several reasons: shape-selective responses were silenced when subjects viewed identical stimuli but their attention was directed away from the shapes to a demanding letter discrimination task; shape-selectivity was present across four different stimulus configurations used to define the figure; LOC responses correlated with participants' reaction times. These results indicate that decision-related activity is present in the LOC when subjects are engaged in threshold-level shape discriminations.

An objective method for measuring face detection thresholds using the sweep steady-state visual evoked response.

We introduce a sensitive method for measuring face detection thresholds rapidly, objectively, and independently of low-level visual cues. The method is based on the swept parameter steady-state visual evoked potential (ssVEP), in which a stimulus is presented at a specific temporal frequency while parametrically varying ("sweeping") the detectability of the stimulus. Here, the visibility of a face image was increased by progressive derandomization of the phase spectra of the image in a series of equally spaced steps. Alternations between face and fully randomized images at a constant rate (3/s) elicit a robust first harmonic response at 3 Hz specific to the structure of the face. High-density EEG was recorded from 10 human adult participants, who were asked to respond with a button-press as soon as they detected a face. The majority of participants produced an evoked response at the first harmonic (3 Hz) that emerged abruptly between 30% and 35% phase-coherence of the face, which was most prominent on right occipito-temporal sites. Thresholds for face detection were estimated reliably in single participants from 15 trials, or on each of the 15 individual face trials. The ssVEP-derived thresholds correlated with the concurrently measured perceptual face detection thresholds. This first application of the sweep VEP approach to high-level vision provides a sensitive and objective method that could be used to measure and compare visual perception thresholds for various object shapes and levels of categorization in different human populations, including infants and individuals with developmental delay.

Distinct effects of attention on the neural responses to form and motion processing: a SSVEP source-imaging study.

We measured neural responses to local and global aspects of form and motion stimuli using frequency-tagged, steady-state visual evoked potentials (SSVEPs) combined with magnetic resonance imaging (MRI) data. Random dot stimuli were used to portray either dynamic Glass patterns (Glass, 1969) or coherent motion displays. SSVEPs were used to estimate neural activity in a set of fMRI-defined visual areas in each subject. To compare activity associated with local versus global processing, we analyzed two frequency components of the SSVEP in each visual area: the high temporal frequency at which the local dots were updated (30 Hz) and the much lower frequency corresponding to updates in the global structure (0.83 Hz). Local and global responses were evaluated in the context of two different behavioral tasks--subjects had to either direct their attention toward or away from the global coherence of the stimuli. The data show that the effect of attention on global and local responses is both stimulus and visual area dependent. When attention was directed away from stimulus coherence, both local and global responses were higher in the coherent motion than Glass pattern condition. Directing attention to coherence in Glass patterns enhanced global activity in areas LOC, hMT+, V4, V3a, and V1, while attention to global motion modulated responses by a smaller amount in a smaller set of areas: V4, hMT+, and LOC. In contrast, directing attention towards stimulus coherence weakly increased local responses to both coherent motion and Glass patterns. These results suggest that visual attention differentially modulates the activity of early visual areas at both local and global levels of structural encoding.

The time course of segmentation and cue-selectivity in the human visual cortex.

Texture discontinuities are a fundamental cue by which the visual system segments objects from their background. The neural mechanisms supporting texture-based segmentation are therefore critical to visual perception and cognition. In the present experiment we employ an EEG source-imaging approach in order to study the time course of texture-based segmentation in the human brain. Visual Evoked Potentials were recorded to four types of stimuli in which periodic temporal modulation of a central 3° figure region could either support figure-ground segmentation, or have identical local texture modulations but not produce changes in global image segmentation. The image discontinuities were defined either by orientation or phase differences across image regions. Evoked responses to these four stimuli were analyzed both at the scalp and on the cortical surface in retinotopic and functional regions-of-interest (ROIs) defined separately using fMRI on a subject-by-subject basis. Texture segmentation (tsVEP: segmenting versus non-segmenting) and cue-specific (csVEP: orientation versus phase) responses exhibited distinctive patterns of activity. Alternations between uniform and segmented images produced highly asymmetric responses that were larger after transitions from the uniform to the segmented state. Texture modulations that signaled the appearance of a figure evoked a pattern of increased activity starting at ∼143 ms that was larger in V1 and LOC ROIs, relative to identical modulations that didn't signal figure-ground segmentation. This segmentation-related activity occurred after an initial response phase that did not depend on the global segmentation structure of the image. The two cue types evoked similar tsVEPs up to 230 ms when they differed in the V4 and LOC ROIs. The evolution of the response proceeded largely in the feed-forward direction, with only weak evidence for feedback-related activity.

Disparity-specific spatial interactions: evidence from EEG source imaging.

Using cortical source estimation techniques based on high-density EEG and fMRI measurements in humans, we measured how a disparity-defined surround influenced the responses to the changing disparity of a central disk within five visual ROIs: V1, V4, lateral occipital complex (LOC), hMT+, and V3A. The responses in the V1 ROI were not consistently affected either by changes in the characteristics of the surround (correlated or uncorrelated) or by its disparity value, consistent with V1 being responsive only to absolute, not relative, disparity. Correlation in the surround increased the responses in the V4, LOC, and hMT+ ROIs over those measured with the uncorrelated surround. Thus, these extrastriate areas contain neurons that are sensitive to disparity differences. However, their evoked responses did not vary systematically with the surround disparity. Responses in the V3A ROI, in contrast, were increased by correlation in the surround and varied with its disparity. We modeled these V3A responses as attributable to a gain modulation of the absolute disparity response, where the gain amplitude is proportional to the center-surround disparity difference. An additional experiment identified a nonlinear center-surround interaction in V3A that facilitates the responses when center and surround are misaligned but suppresses it when they share the same disparity plane.

Increasing the accuracy of electromagnetic inverses using functional area source correlation constraints.

Estimating cortical current distributions from electroencephalographic (EEG) or magnetoencephalographic data is a difficult inverse problem whose solution can be improved by the addition of priors on the associated neural responses. In the context of visual activation studies, we propose a new approach that uses a functional area constrained estimator (FACE) to increase the accuracy of the reconstructions. It derives the source correlation matrix from a segmentation of the cortex into areas defined by retinotopic maps of the visual field or by functional localizers obtained independently by fMRI. These areas are computed once for each individual subject and the associated estimators can therefore be reused for any new study on the same participant. The resulting FACE reconstructions emphasize the activity of sources within these areas or enforce their intercorrelations. We used realistic Monte-Carlo simulations to demonstrate that this approach improved our estimates of a diverse set of source configurations. Reconstructions obtained from a real EEG dataset demonstrate that our priors improve the localization of the cortical areas involved in horizontal disparity processing.

Distinct cortical responses to 2D figures defined by motion contrast.

Motion contrast contributes to the segregation of a two-dimensional figure from its background, yet many questions remain about its neural mechanisms. We measured steady-state visual evoked potential (SSVEP) responses to moving dot displays in which figure regions emerged from and disappeared into the background at a specific temporal frequency (1.2Hz, F1), based on regional differences of dot direction and global direction coherence. The goal was to measure the cortical response function across a range of motion contrast magnitudes. In two experiments using both a low channel count electrode array (Experiment 1) and a high density array (Experiment 2), we observed two distinct phase-locked evoked responses that were similar across motion contrast type. A response at 1.2Hz (1F1) increased in amplitude with increasing magnitudes of direction or coherence contrast. A response at 2.4Hz (2F1) increased in amplitude, but saturated at low levels of direction or coherence contrast. The two components showed different scalp distributions - the 1F1 was strongest along medial occipital channels, while the 2F1 was bilaterally distributed. Taken together, the studies suggest that figures defined by different types of motion contrast are processed by cortical systems with similar dynamics, and that there are separable neural systems devoted to (i) signaling the absolute magnitude of motion contrast and (ii) detecting when a figure defined by motion contrast appears and disappears from view.

Contrast gain control abnormalities in idiopathic generalized epilepsy.

OBJECTIVE: The origin of neural hyperexcitability underlying idiopathic generalized epilepsy (IGE) is not known. The objective of this study is to identify evidence of hyperexcitability in precisely measured visual evoked responses and to understand the nature of changes in excitation and inhibition that lead to altered responses in human patients with IGE. METHODS: Steady-state visual-evoked potentials (VEPs) to contrast reversing gratings were recorded over a wide range of stimulus contrast. VEPs were analyzed at the pattern reversal rate using spectral analysis. Ten patients with IGE and 13 healthy subjects participated. All subjects had normal visual acuity and had no history of photic-induced seizures or photoparoxysmal electroencephalograph (EEG) activity. RESULTS: At a group level, the amplitude of visual responses did not saturate at high stimulus contrast in patients, as it did in the control subjects. This reflects an abnormality in neuronal gain control. The VEPs did not have sufficient power to reliably distinguish patients from controls at an individual level. Parametric modeling using a standard gain control framework showed that the abnormality lay in reduced inhibition from neighboring neurons rather than increased excitatory response to the stimulus. INTERPRETATION: Visual evoked responses reveal changes in a fundamental mechanism regulating neuronal sensitivity. These changes may give rise to hyperexcitability underlying generalized epilepsy.

Disparity-tuned population responses from human visual cortex.

We used source imaging of visual evoked potentials to measure neural population responses over a wide range of horizontal disparities (0.5-64 arcmin). The stimulus was a central disk that moved back and forth across the fixation plane at 2 Hz, surrounded either by binocularly uncorrelated dots (disparity noise) or by correlated dots presented in the fixation plane. Both disk and surround were composed of dynamic random dots to remove coherent monocular information. Disparity tuning was measured in five visual regions of interest (ROIs) [V1, human middle temporal area (hMT+), V4, lateral occipital complex (LOC), and V3A], defined in separate functional magnetic resonance imaging scans. The disparity tuning functions peaked between 2 and 16 arcmin for both types of surround in each ROI. Disparity tuning in the V1 ROI was unaffected by the type of surround, but surround correlation altered both the amplitude and phase of the disparity responses in the other ROIs. Response amplitude increased when the disk was in front of the surround in the V3A and LOC ROIs, indicating that these areas encode figure-ground relationships and object convexity. The correlated surround produced a consistent phase lag at the second harmonic in the hMT+ and V4 ROIs without a change in amplitude, while in the V3A ROI, both phase and amplitude effects were observed. Sensitivity to disparity context is thus widespread in visual cortex, but the dynamics of these contextual interactions differ across regions.